Introduction

Nitrogen (N) is one of the indispensable elements in the whole life cycle of plants, and nitrogen utilization seriously impacts on growth condition and productivity of plants whether in natural or agricultural environment (Xu et al., 2012). There are two beneficial strategies that can be formulated by plants to cope with the deficiencies of nutrition: enhancing nutrient absorption and facilitating nutrient conservation (Aerts and Chapin, 1999). Nutrient absorption is the most essential mechanism for plants to conserve nutrient, which allows plants to make direct re-use of nutrients to adapt to environmental stress (Aerts and Chapin, 1999; Lü et al., 2012). Through this process, plants can transfer a large amount of nutrients from senescent tissues to fresh tissues or other needed tissues (Tully et al., 2013). The formation of nutrient efficiency in plants is a complex process, the percentage of nutrient transport from senescent leaves to green leaves is indicated by nutrient absorption efficiency. Further, NRE (Nitrogen resorption efficiency) and PRE (Phosphorus resorption efficiency) have global averages of ~65 %, and potassium (K) resorption efficiency has global averages of ~70% (Vergutz et al., 2012).

Some studies had reported that increase in nutrient absorption and more effective conservation could change the plant nutrient resorption and their efficiency. Some researchers also reported that the nutrient resorption efficiency differs among habitats (Vergutz et al., 2012), plant species (Diehl et al., 2003; Cai and Bongers, 2007), plant age (Wang et al., 2014), developmental stage (Brant and Chen, 2015), and is easily affected by water and nitrogen content of soil (Lü and Han, 2010). Generally, the process by which plants obtain nutrients from soil is balanced with the process of resorption (Vergutz et al., 2012). The resorption efficiency and resorption proficiency are two merits for the re-use of plants during the process of nutrient resorption (Aerts, 1996). The study reported that a strong resorption is vital for the plant in conditions of nutrient deficiency. Most studies have shown that the relationship about the availability of nutrient and nutrient resorption efficiency is multivariable, and the relationship can be negative (Li et al., 2010b; Vergutz et al., 2012), positive (Yuan et al., 2005) or uninfluenced (Aerts and Chapin, 1999; Yuan and Chen, 2009). One study showed that the addition of N reduced NRE but the change of PRE was not obvious (Lü et al., 2011). Another study had shown that N addition influenced plants PRE (Van Heerwaarden et al., 2003). The nutrients resorption process has a strong link with plant element stoichiometry, since plant growth depends on the availability of nutrients as well as the balance of multiple elements (Ågren, 2008). The resorption can’t regulate the cycling of individual elements but affects multiple elements (Wang et al., 2014). Thus, multiple elements measurement may shed more light on the relationship between RE and elements concentrations rather than individual elements measurement. Meanwhile, plants require mineral elements for normal growth and development, including copper (Cu), calcium (Ca), zinc (Zn), magnesium (Mg), manganese (Mn), iron (Fe), sodium (Na) (Marschner, 2012), and these elements are closely related with crop yield and plant growth, and one element deficiency was usually influenced the other elements metabolism (Liu et al., 2009), for example, improvement of N status would enhance the uptake, remobilization and translocation of Zn in wheat (Erenoglu et al., 2011). The low N probably has influence in mineral balances in plants, further, indirectly or directly regulates mineral contents (Schreiner et al., 2013). Some researchers have indicated that P deficiency increased accumulation of Ca, Fe, Al and Zn, but reduced K and N content (Li et al., 2010a).

Grasses of the sub-family Pooideae are host to endophyte of the genus Epichloë. Endophyte enables the absorption and utilization of plants, and thus thrive in soils low in nutrients (Rahman and Saiga, 2005). Achnatherum inebrians is an invasive grass, which widely distributed in the arid and semi-arid grasslands of northwest China. The feature of this grass is that nearly every plant is infected with a systemic seed-borne fungal endophyte (Chen et al., 2000). Studies have shown that these epichloid endophytes can enhance the resistance of host grasses which are under biotic and abiotic stresses, for instance, it can enhance salt tolerance (Song et al., 2015; Wang et al., 2020), low nitrogen tolerance (Wang et al., 2018a; Wang et al., 2018b; Wang et al., 2020), and Epichloë endophyte influence soil enzymes activity and soil nutrients content in A. inebrians field at the different growth seasons (Hou et al., 2020). However, no research has investigated that the effects of E. gansuensis on the NRE, PRE and KRE, and the content of N, P, K, Na, Mg, Zn, Cu, Ca and Fe in green and senescent leaves of A. inebrians under different N concentrations. Therefore, our study aims would be to test: 1) To determine the concervation of N, P and K in green and senescent leaves, and NRE, PRE and KRE in E+ and E- A. inebrians at different concentrations of N; 2) To determine the ratios of N:P, N:K and P:K, and the contents of Na, Mg, Zn, Cu, Ca and Fe in green and senescent leaves of E+ and E- plants at different N concentrations.

1 Materials and Methods

1.1 Plant growth conditions and nitrogen treatments

E+ and E- A. inebrians seedlings were prepared and treated with the different N concentration as description in our previous study with some modifications (Wang et al., 2018a; Wang et al., 2018b). In short, we used E+ seeds and E- seeds were all originated from a single E+ A. inebrians plant, and half seeds from the single E+ plants were treated with 100 times dilution thiophanate methyl for 2 h, and rinsed the treated seeds with sterile water after that, which was a useful way to kill the endophyte of A. inebrians (Hou et al., 2020), these treated seeds were sowed in the field, and harvested E- seeds, and these E- seeds and the other half seeds of the single E+ plants were used in this study. Sowed 6 healthy and full A.inebrians seeds in 12 pots (E+ plants) and 12 pots (E- plants), respectively. After entering the germination state, each pot (lower diameter (10 cm) × upper diameter (18.5 cm) × height (19.5 cm) kept three seedlings, and prepared two sets of trays for the pots, each tray contains 6 pots. Irrigated all the trays on a seven-day cycle. After the second leaf of A. inebrians seedlings appeared and totally expanded, 1/2 concentration of Hoagland's solution was applied to the pots every 7 days. The greenhouse where these trays were located is constant temperature (temperature: (26±2)°C, moisture: (42±2)%). After 45 days, the modified 1/2 Hoagland's solution containing 0.1 mM N and 7.5 mM N was used to treat 12 pots of E- plants and 12 pots of E+ plants for a further 90 days, and 150 mL of two different N concentrations was applied every 7 days to the corresponding treatment pots. Through the aniline blue method, the seedlings infection status was confirmed. Both E+ and E- plants were applied to each treatment, and each N treatment included six replications.

1.2 The dry weight of green and senescent leaves

After 90 days of treatment, all E+ and E- plants were carefully removed from the vermiculite and the green and senescent leaves were manually separated. To determine the dry weights, green leaves and senescent leaves of each pot of every N treatment were dried in an oven at 80°C until them reached a constant weight.

1.3 Determination of N, P and K content

Flow injection analysis was used to assay the total N and P content in green and senescent leaves (FIAstar 5000 Analyzer, FOSS, Sweden), the method was carried out by the description of Wang et al. (2018b). K content in green leaves and senescent leaves was determined by digital flame analyzer (2655-00, Chicago, USA), the method was performed by the description of Bao et al. (2016). The content of Na, Mg, Zn, Cu, Ca and Fe in green leaves and senescent leaves were analyzed with ICP MS (ICAP RQ), using HF, HNO₃and HCl for digestion for 8 min in 120°C, and then 8 min in 150°C, finally, 30 min in 180°C, volume to 25 mL.

1.4 Calculation of nutrient RE and stoichiometric ratios

The nutrient RE of A. inebrians was calculated with the following formula on the basis of mass (Kobe et al., 2005; Huang et al., 2007): Nutrient RE = ×100%, where Nu_green means the nutrient content in the green leaves and Nu_senescent means the nutrient content in the senescent leaves. E+ and E- ratios of N, P and K in green leaves and senescent leaves of plants were calculated based on N:P, N:K, and P:K.

1.5 Statistical analysis

Under the same N concentration, independent T-test was used to carry out the significance of difference for the all parameters of E+ and E- plants, and the significance of difference between green leaves and senescent leaves for all parameters was conducted by independent T-tests under the same N concentration. The statistical significance was defined at the 95% confidence level. Mean value are expressed as its standard errors. Principal component analysis was performed with the content of N, P, K, Na, Mg, Zn, Cu, Ca and Fe by R. The two-way ANOVA analyzed the effects of endophyte (E) and N concentration (NC) on NRE, PRE and KRE, the three-way ANOVA analyzed the effects of endophyte (E), nitrogen concentration (NC), and tissues (T) on the contents of N, P, K, Na, Mg, Zn, Cu, Ca and Fe, and the ratios of N:P, N:K and P:K.

2 Results

2.1 Dry weights of green and senescent lamina of E+ and E- plants

After 90 days of treatment with two concentrations of external nitrogen, our results showed that the dry weight of E+ and E- green leaves of under 0.1 mM N treatment was significantly reduced compared to 7.5 mM N (Figure 1), but the present of E. gansuensisincreased the dry weight of green leaves compared to E- green leaves under 0.1 mM N. Further, low-N stress significantly increased the dry matter of senescent leaves in E+ and E- plants compared to the 7.5 mM N (Figure 1). The dry weight of senescent leaves had no significant differences between E+ and E- plants under 0.1 mM N and 7.5 mM N, respectively. The dry weight of green leaves was higher than senescent leaves in E+ and E- plants under 7.5 mM N, however, the dry weight of senescent leaves was lower than green leaves in E+ plants under low N condition.

2.2 The effect of E. gansuensis on the content of N, P and K of the green and senescent leaves under the different N concentration

The N, P and K content of green leaves was higher than senescent leaves in E+ and E- plants under two N concentrations, respectively. Further, our results indicated that 0.1 mM N decreased the content of N, P and K of E+ and E- plants compared with the 7.5 mM N (Figure 2). However, the N content of green and senescent leaves, and P content of green leaves had obvious differences between E+ and E- plants under 0.1 mM N (Figure 2a; Figure 2b). The N and P content of the green leaves of E- plants were lower than the counterparts of E+ plants under low N condition, and N and P content of the green leaves of E+ plants were enhanced by 19.9% and 12.7% compared with the green leaves of E- plants under 0.1 mM N, respectively (Figure 2a). The N content of the senescent leaves in E+ plants was lower than the counterparts of E- plants under 0.1 mM N (Figure 2a), and the N content of the senescent leaves of E+ plants was decreased by 11.9% compared with the senescent leaves of E- plants under 0.1 mM N (Figure 2a). There was no obvious difference in K content in green leaves of E+ and E- plants under 0.1 mM N and 7.5 mM N, the result was consistent with the K content of senescent leaves (Figure 2c). As shown in Table 1, the endophyte-infection did not cause a remarkable effect on the content of N, P and K, while nitrogen concentration (NC) and the tissues (T) caused marked effects on the content change of N, P and K, respectively (P<0.001). In addition, the interaction of NC × T had clear differences on the content of N (P<0.001) and K (P=0.016).

2.3 The effect of E. gansuensis on NRE, PRE and KRE of A. inebrians at the various N concentrations

The presence of E. gansuensis increased NRE compared to E- plants under 0.1 mM N, and NRE of E+ plants were enhanced by 27.4 % compared with those of E- plants under 0.1 mM N (Figure 3a). However, NPE PRE and KRE had not affected by endophyte, under normal N condition (Figure 3). The PRE and KRE had no obvious differences between E+ plants and E- plants under 0.1 mM N (Figure 3b; Figure 3c). NC caused obvious effects on the NRE (P=0.049) and PRE (P<0.001) (Table 2). 

2.4 The ratios of N:P, N:K and P:K of the green leaves and senescent leaves in E+ and E- plants

The content of N, P and K of the green and senescent leaves were distinct, thus their ratios also varied differently (Figure 4). Our research shown that 0.1 mM N decreased the ratios of N:P and N:K of the green leaves compared with 7.5 mM N in E+ plants and E- plants (Figure 4a; Figure 4b), and 0.1 mM N decreased P:K ratio of the senescent leaves compared with 7.5 mM N in E+ plants and E- plants (Figure 4c). The N:P ratio of the green leaves and the N:K ratio of the green leaves had clear differences between E+ and E- plants, respectively, under 0.1 mM N (Figure 4a; Figure 4b), with the N:P ratio of the green leaves in E+ plants increased by 8.49% compared with the green leaves of E- plants. The data also had shown that the N:K ratio of the green leaves in E+ plants was decreased by 22.65% compared with the counterpart of E- plants under 0.1 mM N (Figure 4b). Furthermore, Table 1 showed that the endophyte did not have effect on the ratios of N:P, N:K and P:K, while NC caused the notable effects on the ratios of N:P (P<0.001) and N:K (P<0.001), and T also caused the marked effects on the ratios of N:P (P<0.001), N:K (P<0.001) and P:K (P<0.001). In addition, the interaction of NC × T had clear differences on the ratio of N:P (P<0.001), N:K (P<0.001) and P:K (P=0.003).

2.5 The effect of E. gansuensis on the content of metal ion in green leaves and senescent leaves under the various N concentrations

The content of Na, Mg and Ca of the green leaves was dramatically lower than the senescent leaves in E+ and E- plants under the two N concentrations, respectively (Figure 5a; Figure 5b; Figure 5e). We also found that the contents of Zn and Cu of the green leaves were both significantly higher than the senescent leaves in E+ and E- plants under low N treatment (Figure 5c; Figure 5d). Under 7.5 mM N, the Fe content of the green leaves was remarkably lower than the senescent leaves in E+ and E- plants (Figure 5f). Further, E. gansuensismarkedly reduced the Zn content of green leaves compared with the counterpart of E- plants under 0.1 mM N (Figure 5c), but E. gansuensis clearly increased the content of Na, Mg, Zn, Cu, Ca and Fe of green leaves compared with the counterpart of E- plants under 7.5 mM N. E. gansuensis significantly decreased the content of Na, Mg, Zn and Ca of senescent leaves compared with the counterpart of E- plants under 7.5 mM N, however, E. gansuensis enhanced the content of Na, Mg, Zn and Ca of senescent leaves compared with the counterpart of E- plants under low N treatment (Figure 5). Table 3 demonstrated that endophyte had significant effect on the content of Cu (P<0.001), Ca (P<0.001) and Fe (P<0.001), while NC caused clear effects on the content of Na (P<0.001), Mg (P<0.001), Zn (P<0.001) and Cu (P<0.001). In addition, the interaction of E × NC × T had clear differences on the content of Na (P<0.001), Mg (P<0.001), Zn (P<0.001), Cu (P=0.028) and Ca (P<0.001).

2.6 Principal component analysis

Some variables represented distinct separation, and the factor 1 could explain 50.39% of the total variance in green leaves, on which Cu content contributed the most variation (45.7%), while Mg content and Zn content accounted for approximately 44.7% and 41.5%, respectively (Figure 6). N content (50.9%) and K content (46.2%) were loaded on factor 2, which could explain 39.15% of the variation. The difference between 0.1mM and 7.5 mM N from E+ and E- plants could be seen in the PCA plot (Figure 6). However, distinct separation of some variables was showed, and in senescent leaves, 68.48% of the total variance was explained by factor 1, on which Mg content contributed the most variation (37.0%), while P and Zn content accounted for approximately 36.6% and 36.0%, respectively (Figure 7). Cu content (52.5%) and Na content (48.5%) were loaded on factor 2, and which could explain 20.98% of the variation. The differences between 0.1 mM N and 7.5 mM N from E+ plants and E- plants were shown by PCA plot (Figure 7).

3 Discussion

Based on our research results, the E. gansuensis enhanced the adaptation of the host grass to low N stress, and it included the dry weight of green leaves in E+ plants were higher than the counterpart of E- plants. However, the dry weight of senescent leaves was not affected by endophyte when the plant suffers from low nitrogen stress. Some studies also showed that the E. gansuensis had powerful biological functions and improved A. inebrians resistance to abiotic stresses, and increased dry weight of host grasses compared to E- plants (Wang et al., 2018a; Wang et al., 2018b), therefore, our present results were coincident with the previous results.

Some previous studies had reported that with the nitrogen supply increased, the NRE of some ecosystems remained unchanged or decreased (Van Heerwaarden et al., 2003; Güsewell, 2005b; Kozovits et al., 2007) However, the other study indicated that the addition of N caused plants to show a specific PRE response (Van Heerwaarden et al., 2003). One study concluded that the resorption efficiency of plant specific nutrient might not have much to do with nutrient status (Aerts, 1996). Additionally, the degree of senescence might partly contribute to the low RE, and elements also might be through the production and decomposition of leaf litter back into the soil. However, some of the elements from senescent leaves were translocated to other tissues of plants in the later stages of senescence (Blanco et al., 2009; Lü et al., 2012). There were no study reports that the roles of E. gansuensis endophyte on nutrient resorption efficiency of host grasses under different N concentration. Current research shown that, both NRE of E- plant and KRE of E+ plant was affected by N supply. Our results suggested that compared with E- plants, E. gansuensis increased host plants NRE under 0.1 mM N stress, which indicated more N was transferred from the senescent leaves and reused in green leaves of E+ plants under 0.1 mM N condition; however, the infection of E. gansuensis did not affect the PRE and KRE of host grasses under the two different N treatments. Improvement of N utilization efficiency in the plants will enhance plant growth under low N stress.

N, P and K are very important elements for plant growth (Amtmann and Rubio, 2012), and as the plant grows, the contents of N, P and K in leaves are constantly changing (Alam et al., 2011). The balance of nutrients can influence plant growth rates, and the N, P and K ratio in ecosystems has been widely studied (Wang et al., 2014; Scalon et al., 2017). In the current study, we investigated different responses of E+ and E- A. inebrians to low N conditions and analyzed the possible changes of C, N and P content in green and senescent leaves. Few studies have revealed the effect of endophyte on difference of N concentration from the perspective of N, P, K ratio. In this study, there were effects of E. gansuensis on the N content of green and senescent leaves and the P content of green leaves under 0.1 mM N. Further, our study indicated that the presence of E. gansuensis increased N and P content of the green leaves but decreased the N content of the senescent leaves under 0.1 mM N. Recently, it was reported that an epichloid endophyte increased the P and N content in Hordeum brevisubulatum plants under NaCl stress (Song et al., 2015; Chen et al., 2018). A previous study had shown that E. coenophila(Neotyphodium coenophialum) affected mineral absorption, transportation and nutrient ratios of tall fescue (Festuca arundinacea) (Rahman and Saiga, 2005). Similarly, E. festucae changed the nutrient composition of F. rubra, and the content of P (62%) and N (19%) in E+leaves were more than E- plants (Vázquez-de-Aldana et al., 2013). This study had provided evidence that the existence of epichloid endophytes in grasses can affect the availability of nutrients to growing leaves of host grasses through enhanced resorption from senescent leaves to improve host adaptability to environment conditions. All in all, the existence of E. gansuensis increased the NRE of A. inebrians to improve host grasses growth under N deficiency stress, and to enhance the nutrient use efficiency in the case of limited nutrients. Due to changes of N, P and K content, there was only change for the N:P ratio of the green leaves under 0.1 mM N.

There are conclusions about the relationships between plant resorption process and nutrition status (Diehl et al., 2003; Kobe et al., 2005; Vergutz et al., 2012), for example, according to the reports, in mature leaf nitrogen content was positively correlated with the absorption of nitrogen in forests. (Diehl et al., 2003). However, it was found that an increase in nutritional status was globally associated with a decrease in NRE, PRE and KRE (Kobe et al., 2005; Vergutz et al., 2012). Meanwhile, several studies have reported that N and P interact functionally, NRE and PRE are tightly coupled (Güsewell, 2005a; Ågren, 2008). Although plants growing in poor environment always had longer leaf life and lower nutrient concentration, the negative correlation between nutrient availability and NRE has not proven to be a consistent property (Kobe et al., 2005). Low-N stress and E. gansuensis also influenced the related elements of photosynthesis, for example, the net photosynthetic rate, chlorophyll a and chlorophyll b (Wang et al., 2018a). Fe is also related with the ability of carbon assimilation, and it plays an essential role in the chlorophyll synthesis in photosynthesis. The results come from our research showed that E. gansuensis enhanced the green leaves Fe content under 7.5 mM N, and Fe is a coenzyme factor of NR (nitrate reductase), NiR (nitrite reductase) and GS (glutamate synthase) in the pathway of N metabolism (Borlotti et al., 2012), interestingly, E. gansuensis increased the activity of NR, NiR and GS under 0.1 mM N (Wang et al., 2018b). Zn is also important element for the synthesis of chlorophyll. In E+ plants, N deficiency reduced Zn content of green leaves, but low N improved Zn content of green leaves of. E. gansuensis probably play an essential role in regulating the balance of iron to improve host grasses growth under the environment stress.

In nutrient-poor environments, the efficiency of nutrient recycling affects plants growth and reproduction (May and Killingbeck, 1992). Plants vary greatly in the efficiency with which nutrients are resorbed before leaf abscission. In our study, there was remarkable positive correlation between dry weight of green leaves and KRE in E+ plants, and there was also significant positive correlation between the dry weight of senescent leaves and PRE in E+ plants. e However, in E- plants, there was no obvious relationship between dry weight of leaves and REs. Therefore, it seems to be generally true that the presence of the endophyte affected the correlation between leaves dry weight and REs.

In summary, E. gansuensis played an important role on increasing NRE, the content N and P of green leaves under 0.1 mM N, and influencing the content of Na, Mg, Zn, Cu, Ca and Fe of the green leaves and senescent leaves to improve A. inebrians growth under low-N stress. The present study highlight that it is meaningful to investigate the responses of host plants to E. gansuensis, not only to elucidate the role of endophyte but also to understand the nutrients resorption from the senescent leaves to green leaves. Our results had expanded the biological functions of E. gansuensis endophyte, and E. gansuensican be used to cultivate new forage germplasm with high nutrient re-absorption efficiency in the future.

Author contributions

CC, WJF conceived and designed the research. CC, WJF, LRG, HWP performed the research. CC, LYL, WJF participated in the experiments and analyzed data. CC, WJF, MJC drafted and revised the manuscript. All authors read and approved the final manuscript.

Acknowledgements

This research was financially supported by Program for Changjiang Scholars and Innovative Research Team in University (IRT_17R50), the Joint Fund of the Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province (Grant No. U1812401), the Natural Science Foundation of China (32001399, 32001387, 31971768), the Technical Service Agreement for Research and Development of Beneficial Microbial Agents of Rhododendron Alpine (071200001), Lanzhou University “Double First-Class” guiding special project-team construction fund-scientific research start-up fee standard (561119206), the Fundamental Research Funds for the Central Universities (lzujbky-2021-ey01, lzujbky-2021-kb12) in Lanzhou University, the Open Project of State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (2021-KF-02).

Competing interests

The authors declare that they have no competing interests

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